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PMID: 20083601 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Pincher-generated Nogo-A endosomes mediate growth cone collapse and retrograde signaling.

The Journal of cell biology ·Vol. 188 ·No. 2 ·2010-01-25 ·Pages 271-85

Joset A, Dodd DA, Halegoua S, Schwab ME

Abstract

Nogo-A is one of the most potent myelin-associated inhibitors for axonal growth, regeneration, and plasticity in the adult central nervous system. The Nogo-A-specific fragment NogoDelta20 induces growth cone collapse, and inhibits neurite outgrowth and cell spreading by activating RhoA. Here, we show that NogoDelta20 is internalized into neuronal cells by a Pincher- and rac-dependent, but clathrin- and dynamin-independent, mechanism. Pincher-mediated macroendocytosis results in the formation of NogoDelta20-containing signalosomes that direct RhoA activation and growth cone collapse. In compartmentalized chamber cultures, NogoDelta20 is endocytosed into neurites and retrogradely transported to the cell bodies of dorsal root ganglion neurons, triggering RhoA activation en route and decreasing phosphorylated cAMP response element binding levels in cell bodies. Thus, Pincher-dependent macroendocytosis leads to the formation of Nogo-A signaling endosomes, which act both within growth cones and after retrograde transport in the cell body to negatively regulate the neuronal growth program.

MeSH Terms
Animals Axonal Transport/physiology Cell Differentiation/physiology Cells, Cultured Cyclic AMP/metabolism Diffusion Chambers, Culture Endocytosis/physiology Endosomes/metabolism,ultrastructure Ganglia, Spinal/embryology,metabolism,ultrastructure Growth Cones/metabolism,ultrastructure Myelin Proteins/genetics,metabolism Nerve Tissue Proteins/genetics,metabolism Neurogenesis/physiology Nogo Proteins Organ Culture Techniques PC12 Cells Phosphorylation Rats Sensory Receptor Cells/metabolism,ultrastructure Signal Transduction/physiology rhoA GTP-Binding Protein/genetics,metabolism
Chemicals
Ehd4 protein, rat Myelin Proteins Nerve Tissue Proteins Nogo Proteins Rtn4 protein, rat Cyclic AMP rhoA GTP-Binding Protein
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Joset Armela
Brain Research Institute, University of Zurich, Zurich, Switzerland. hatkic@hifo.uzh.ch
Dodd Dana A
Halegoua Simon
Schwab Martin E
References (78)
78 references, click to expand
  1. Pathways of clathrin-independent endocytosis.
    Nat Rev Mol Cell Biol. 2007 Aug;8(8):603-12 PMID: 17609668
  2. Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord.
    J Neurosci. 2002 Aug 15;22(16):7097-110 PMID: 12177206
  3. Trk-signaling endosomes are generated by Rac-dependent macroendocytosis.
    Proc Natl Acad Sci U S A. 2007 Jul 24;104(30):12270-5 PMID: 17640889
  4. Soluble Nogo-A, an inhibitor of axonal regeneration, as a biomarker for multiple sclerosis.
    Neurology. 2007 Jan 23;68(4):283-7 PMID: 17242333
  5. Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans.
    J Neurosci. 1999 Oct 15;19(20):8979-89 PMID: 10516316
  6. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones.
    Cell. 1993 Oct 22;75(2):217-27 PMID: 8402908
  7. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury.
    Neuron. 2004 Oct 28;44(3):439-51 PMID: 15504325
  8. A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein.
    Nat Neurosci. 2002 Dec;5(12):1302-8 PMID: 12426574
  9. Application of neutralizing antibodies against NI-35/250 myelin-associated neurite growth inhibitory proteins to the adult rat cerebellum induces sprouting of uninjured purkinje cell axons.
    J Neurosci. 2000 Mar 15;20(6):2275-86 PMID: 10704503
  10. Culturing hippocampal neurons.
    Nat Protoc. 2006;1(5):2406-15 PMID: 17406484
  11. Regulated cleavage of a contact-mediated axon repellent.
    Science. 2000 Aug 25;289(5483):1360-5 PMID: 10958785
  12. Structure of the Nogo receptor ectodomain: a recognition module implicated in myelin inhibition.
    Neuron. 2003 Apr 24;38(2):177-85 PMID: 12718853
  13. Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion.
    Nat Cell Biol. 2003 Oct;5(10):879-88 PMID: 12973357
  14. Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival.
    Nat Cell Biol. 2008 Feb;10(2):149-59 PMID: 18193038
  15. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae.
    Science. 2002 Apr 19;296(5567):535-9 PMID: 11964480
  16. Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling.
    Nat Cell Biol. 2001 Jun;3(6):573-9 PMID: 11389442
  17. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III.
    Cell. 1997 Aug 22;90(4):739-51 PMID: 9288753
  18. Function of an axonal chemoattractant modulated by metalloprotease activity.
    Science. 2000 Aug 25;289(5483):1365-7 PMID: 10958786
  19. AP-2/Eps15 interaction is required for receptor-mediated endocytosis.
    J Cell Biol. 1998 Mar 9;140(5):1055-62 PMID: 9490719
  20. Structure and axon outgrowth inhibitor binding of the Nogo-66 receptor and related proteins.
    EMBO J. 2003 Jul 1;22(13):3291-302 PMID: 12839991
  21. Neuropilin is a semaphorin III receptor.
    Cell. 1997 Aug 22;90(4):753-62 PMID: 9288754
  22. Vav family GEFs link activated Ephs to endocytosis and axon guidance.
    Neuron. 2005 Apr 21;46(2):205-17 PMID: 15848800
  23. EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion.
    Nat Cell Biol. 2003 Oct;5(10):869-78 PMID: 12973358
  24. Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates--re-examination and extension of behavioral data.
    Eur J Neurosci. 2009 Mar;29(5):983-96 PMID: 19291225
  25. The coming of age of axonal neurotrophin signaling endosomes.
    J Proteomics. 2009 Feb 15;72(1):46-55 PMID: 19028611
  26. Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex.
    J Neurosci. 1999 Sep 15;19(18):7889-900 PMID: 10479691
  27. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles.
    J Cell Biol. 2005 Jan 31;168(3):465-76 PMID: 15668297
  28. Molecular approaches to spinal cord repair.
    Annu Rev Neurosci. 2003;26:411-40 PMID: 12626698
  29. Retrograde transport of neurotrophins: fact and function.
    J Neurobiol. 2004 Feb 5;58(2):217-29 PMID: 14704954
  30. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals.
    Neuron. 2003 Jul 3;39(1):69-84 PMID: 12848933
  31. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS.
    Nat Rev Neurosci. 2003 Sep;4(9):703-13 PMID: 12951563
  32. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex.
    Nat Neurosci. 2004 Mar;7(3):221-8 PMID: 14966521
  33. Schwann cell-derived factor-induced modulation of the NgR/p75NTR/EGFR axis disinhibits axon growth through CNS myelin in vivo and in vitro.
    Brain. 2006 Jun;129(Pt 6):1517-33 PMID: 16613894
  34. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif.
    J Biol Chem. 1995 Jun 2;270(22):13503-11 PMID: 7768953
  35. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes.
    J Cell Biol. 2002 May 13;157(4):679-91 PMID: 12011113
  36. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium.
    J Cell Biol. 1998 Apr 6;141(1):101-14 PMID: 9531551
  37. An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons.
    Science. 1997 Aug 22;277(5329):1097-100 PMID: 9262478
  38. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact.
    J Neurosci. 2002 Jul 1;22(13):5505-15 PMID: 12097502
  39. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway.
    Neuron. 2001 Dec 6;32(5):801-14 PMID: 11738027
  40. Neuronal Nogo-A modulates growth cone motility via Rho-GTP/LIMK1/cofilin in the unlesioned adult nervous system.
    J Biol Chem. 2009 Apr 17;284(16):10793-807 PMID: 19208621
  41. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates.
    Cell. 1999 Oct 1;99(1):71-80 PMID: 10520995
  42. Local control of neurite development by nerve growth factor.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4516-9 PMID: 270699
  43. Cell-autonomous mechanisms and myelin-associated factors contribute to the development of Purkinje axon intracortical plexus in the rat cerebellum.
    J Neurosci. 2003 Jun 1;23(11):4613-24 PMID: 12805301
  44. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein.
    Nature. 2000 Jan 27;403(6768):439-44 PMID: 10667797
  45. Evidence that dynamin-2 functions as a signal-transducing GTPase.
    J Cell Biol. 2000 Jul 10;150(1):145-54 PMID: 10893263
  46. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling.
    Nat Rev Mol Cell Biol. 2005 Feb;6(2):112-26 PMID: 15687999
  47. pH and the recycling of transferrin during receptor-mediated endocytosis.
    Proc Natl Acad Sci U S A. 1983 Apr;80(8):2258-62 PMID: 6300903
  48. Cell-derived proteases and protease inhibitors as regulators of neurite outgrowth.
    Trends Neurosci. 1988 Dec;11(12):541-4 PMID: 2471310
  49. Neuronal dynamics and axonal flow. IV. Blockage of intra-axonal enzyme transport by colchicine.
    Proc Natl Acad Sci U S A. 1969 Mar;62(3):722-8 PMID: 4184255
  50. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates.
    Nat Med. 2006 Jul;12(7):790-2 PMID: 16819551
  51. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo.
    Neuron. 2004 Nov 18;44(4):609-21 PMID: 15541310
  52. Pincher-mediated macroendocytosis underlies retrograde signaling by neurotrophin receptors.
    J Neurosci. 2005 May 25;25(21):5236-47 PMID: 15917464
  53. Signaling mechanisms of the myelin inhibitors of axon regeneration.
    Curr Opin Neurobiol. 2003 Oct;13(5):545-51 PMID: 14630216
  54. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration.
    Nature. 2001 Jan 18;409(6818):341-6 PMID: 11201742
  55. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats.
    Ann Neurol. 2005 Nov;58(5):706-19 PMID: 16173073
  56. Inhibitor of neurite outgrowth in humans.
    Nature. 2000 Jan 27;403(6768):383-4 PMID: 10667780
  57. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton.
    EMBO J. 1999 Feb 1;18(3):578-85 PMID: 9927417
  58. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells.
    Cell. 1983 Nov;35(1):321-30 PMID: 6313227
  59. Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1.
    J Neurosci. 2002 Dec 1;22(23):10368-76 PMID: 12451136
  60. Nogo-66 receptor antagonist peptide promotes axonal regeneration.
    Nature. 2002 May 30;417(6888):547-51 PMID: 12037567
  61. Effectors for the Rho GTPases.
    Curr Opin Cell Biol. 1999 Feb;11(1):95-102 PMID: 10047515
  62. Glial inhibition of CNS axon regeneration.
    Nat Rev Neurosci. 2006 Aug;7(8):617-27 PMID: 16858390
  63. Nogo and axon regeneration.
    Curr Opin Neurobiol. 2004 Feb;14(1):118-24 PMID: 15018947
  64. A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane.
    EMBO J. 2002 Jun 3;21(11):2557-67 PMID: 12032069
  65. Neurotrophins: roles in neuronal development and function.
    Annu Rev Neurosci. 2001;24:677-736 PMID: 11520916
  66. The Nogo-Nogo receptor pathway limits a spectrum of adult CNS axonal growth.
    J Neurosci. 2006 Nov 22;26(47):12242-50 PMID: 17122049
  67. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions.
    J Neurosci. 2003 Jul 2;23(13):5393-406 PMID: 12843238
  68. Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells.
    Cell. 1990 Aug 24;62(4):719-31 PMID: 2143699
  69. The function of dynamin in endocytosis.
    Curr Opin Neurobiol. 1995 Oct;5(5):559-65 PMID: 8580706
  70. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions.
    J Neurosci. 2002 May 1;22(9):3553-67 PMID: 11978832
  71. Retrograde neurotrophin signaling: Trk-ing along the axon.
    Curr Opin Neurobiol. 2002 Jun;12(3):268-74 PMID: 12049932
  72. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor.
    Science. 2005 Sep 30;309(5744):2222-6 PMID: 16195464
  73. PirB is a functional receptor for myelin inhibitors of axonal regeneration.
    Science. 2008 Nov 7;322(5903):967-70 PMID: 18988857
  74. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling.
    Nature. 2007 Oct 18;449(7164):923-7 PMID: 17914359
  75. Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones.
    Science. 1993 Jan 1;259(5091):80-3 PMID: 8418499
  76. The detection and quantification of growth cone collapsing activities.
    Nat Protoc. 2007;2(8):2005-11 PMID: 17703212
  77. Long-distance retrograde neurotrophic signaling.
    Curr Opin Neurobiol. 2005 Feb;15(1):40-8 PMID: 15721743
  78. Rho kinase inhibition enhances axonal regeneration in the injured CNS.
    J Neurosci. 2003 Feb 15;23(4):1416-23 PMID: 12598630
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
Published
2010-01-25
Epub
2010-00-18
Pages
271-85
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2812518
Subset
IM
Grants
NINDS NIH HHS · R01 NS018218 · United States
NINDS NIH HHS · NS18218 · United States
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